European Standards and North American Practice Parameters for Skin Prick Testing Panels in Allergic Rhinitis and Asthma

Home , Aeroallergen, Parietaria, Parietaria judaica

Romanian Journal of Rhinology, Vol. 5, No. 17, January-March 2015 DOI: 10.1515/rjr-2015-0002 LITERATURE REVIEW European standards and North American practice parameters for skin prick testing panels in allergic rhinitis and asthma

Florin-Dan Popescu Department of Allergology, “Carol Davila” University of Medicine and Pharmacy, Bucharest, Romania

ABSTRACT

According to the Global Allergy and Asthma European Network (GA²LEN), a pan-European skin prick test panel for the diagnosis of allergic rhinitis and asthma includes 18 aeroallergen extracts, supplemented if necessary for regional or for particular patient needs, while the Allergen Subcommittee and Immunotherapy Committee of the American Academy of Allergy, Asthma and Immunology (AAAAI) selected 36 major clinically relevant aeroallergens for North America. KEYWORDS: aeroallergen extracts, skin prick tests, allergic rhinitis and asthma

INTRODUCTION PARAMETERS FOR SKIN PRICK TESTING PANELS Skin prick testing is an important reliable method to diagnose IgE-mediated allergic rhinitis, rhinocon- The aeroallergen extracts included in the Euro- junctivitis and asthma. This widely used in vivo assess- pean standards and North American practice param- ment, indicated, performed and interpreted by al- eters skin prick panels are of plant, fungal and ani- lergy practitioners, is minimally invasive, has immedi- mal origins, as described below1-8. ately available and reproducible results, and provides Aeroallergen extracts of animal origin included in evidence for aeroallergen sensitization. Skin prick these standards belong to Arthropoda phylum, Astig- tests are highly specific and sensitive for the diagnosis mata order (house dust mites from the Pyroglyphidae of respiratory allergies. The positive predictive value family), Blattodea order (Ectobiidea family from the to diagnose allergic rhinitis increases to 97-99% if al- Insecta class), and Carnivora order pet animals (Felidae lergy skin prick testing is utilized1,2. and Canidae families). According to the Global Allergy and Asthma Euro- Allergen extracts of fungal origin mentioned in pean Network (GA²LEN), a pan-European skin prick the European and North American recommenda- test panel for the diagnosis of allergic rhinitis and tions belong to moulds from the phylum Ascomycota asthma includes 18 aeroallergen extracts, and these (Dothideomycetes and Eurothiomycetes classes). allergens can be supplemented, if necessary, for re- Pollen from trees or shrubs from Fagales order gional or for particular patient needs2. The Allergen (Betulaceae and Fagaceae families), Malpighiales order Subcommittee and Immunotherapy Committee of (Salicaceae family), Lamiales order (Oleaceae family), the American Academy of Allergy, Asthma and Im- Proteales order (Platanaceae family), Sapindales order munology (AAAAI) previously compiled and selected (Aceraceae family), Rosales order (Moraceae and Ul- 36 key aeroallergens in North America3. maceae families), and Coniferales order (Cupressaceae family), grass pollen from Poales order, Poaceae

Corresponding author: Florin-Dan Popescu, MD, PhD, Associate Professor, Head of Department of Allergology, “Carol Davila” University of Medicine and Pharmacy, Bucharest, Romania; Address: “Nicolae Malaxa” Clinical Hospital, 12 Sos. Vergului, Bucharest, Sector 2, Romania e-mail: [email protected] 20 Romanian Journal of Rhinology, Vol. 5, No. 17, January-March 2015

(gramineae) family (Pooideae, Chloridoideae and Pani- Aeroallergens of animal origin, such as those from coideae subfamilies), and pollen from weeds belong- house dust mites, domestic pets and insects, are im- ing to Asterales order (Asteraceae / Compositae family), portant indoor allergens involved in allergic rhinitis Rosales order (Urticaceae family), Lamiales order (Plan- and asthma as discussed below1-3,6-8,17,25-30. Spending taginaceae family), Caryophyllales order (Polygonaceae more time inside buildings (at work and at home) and Amaranthaceae / Chenopodiaceae families) are in- creates conditions for more exposure to multiple included in these panels. door aeroallergens. House dust includes various or- Weather and climate change the impact of aeroal- ganic and inorganic matter, including dust mites, lergens in Europe and North America6,9-12, particu- animal dander, cockroach debris and other insect larly pollens and moulds. Climatological regimes parts, natural and synthetic fibers, but also moulds, (warm or cold anomalies, dryer and wetter periods), pollen grains and inorganic debris. House dust mites along with meteorological factors (temperature, are the most common and important indoor aller- wind speed, humidity, rain, thunderstorms), are in- gens. volved. It is known that human activities increase at- House dust mites belong to the phylum of Arthrop- mospheric greenhouse gases, such as carbon dioxide. oda (class Arachnida, subclass Acari), Astigmata order, Over the last decades, raised temperatures and at- Pyroglyphidae family, and the most important species mospheric carbon dioxide concentration have im- are Dermatophagoides pteronyssinus and Dermatophagoi- pacted plant and pollen distribution, and induced des farinae, and this is the reason why allergen extracts changes in the quantitative production and disper- of these domestic mites are included in European sion of pollen, pollen season periods and allergen standards and North American practice parameters content of pollen grains, which may be region- and skin prick panels. Pyroglyphid mites are highly cross- species-specific. During the last decades, several reactive, but they seem to have a limited cross-reactiv- changes described below were observed6,13-24. Some ity with storage mites found in farms, and Blomia anemophilous plants pollinate earlier, the duration tropicalis, significant mite species in tropical or sub- of the pollen season is extended in some species, and tropical areas. These non-pyroglyphid mite extracts there are more days with greater airborne pollen are used only in selected cases, and are not included grain concentrations. Production of allergenic pollen in pan-European and North American screening of some weeds is increased with high ambient carbon panels. dioxide levels. Moreover, higher daily temperatures The most important urban indoor inhalant insect may increase pollen allergenicity. Climate changes allergens in Europe and North America derive from may also lead regionally to the extinction of some domestic cockroach species, especially Blattella ger- plant species and to the proliferation of non-native manica (German cockroach), this one being included alien species with allergenic pollens. in North American and European standard panels. According to standardized skin prick testing per- Aeroallergens of small mammal pets from the Car- formed at excellence centres in European countries, nivora order (epithelia/dander) belong to the Felidae the Global Allergy and Asthma European Network family: Felis catus syn. Felis domesticus (domestic cat) (GA²LEN) in association with the European Acad- and Canidae family: Canis lupus familiaris syn. Canis emy of Allergy and Clinical Immunology (EAACI) familiaris (dog). Both are included in European and suggested a panel of aeroallergens for skin prick test- North American practice parameters skin prick pan- ing in all European patients. As mentioned before, els. In selected cases, other mammalian allergen ex- allergen extracts can be supplemented if necessary tracts may be used (horse, domestic guinea pig, ham- for regional or for particular patient needs2. The ster, rabbit). American Academy of Allergy, Asthma and Immunol- Aeroallergens of fungal origin involved in allergic ogy (AAAAI) previously selected a double number of sensitization in rhinitis and asthma1-3,6-8,17,31-34 are key aeroallergens in North America compared with moulds belonging to the phylum Ascomycota, class actual European standard. For an individual patient, Dothideomycetes, Pleosporaceae family: Alternaria alternata the choice of allergen extracts for skin prick testing syn. Alternaria tenuis, Davidielaceae family: Cladosporium should be guided primarily by the patient’s detailed herbarum, Cladosporium cladosporioides (both types history and physical examination, by the sciences of being predominantly outdoor moulds, with dry aerobiology, botany, mycology, arthropod biology, spores), and class Eurothiomycetes, Trichocomaceae fam- and the contact with companion animals. In North ily: Aspergillus fumigatus (predominantly indoor America, it is not possible to elaborate a universal list mould). Alternaria alternata, Cladosporium spp and As- of appropriate aeroallergens for skin prick testing in pergillus fumigatus are included in North American all patients. The selection of allergen extracts for in and European standard panels. The North American vivo testing reflects the physician’s knowledge, train- practice parameters skin prick panel includes in ad- ing and experience3. dition fungi belonging to class Eurothiomycetes, Tricho- Popescu European standards and North American practice parameters for skin prick testing panels in allergic rhinitis and asthma 21 comaceae family: Penicillium chrysogenum syn. Penicil- spread in the temperate zone; their pollen represents lium notatum, Penicillium expansum, and dematiaceous a substantial proportion of grass pollen grains to fungi from class Dothideomycetes: Bipolaris/Curvularia/ which European and American rhinitis patients are Drechslera spicifera syn. Helminthosporium spiciferum, sensitized, and their pollen extracts are included in and Epicoccum nigrum syn. Epicoccum purpurascens the grass pollen mixes used for skin prick testing. (predominantly indoor moulds). Other Pooideae grasses included in some mixes are Pollens of anemophilous plants (wind-pollinated Festuca pratensis syn. Festuca elatior (meadow fescue), plants) are important outdoor sources of aeroaller- Holcus lanatus (velvet grass or Yorkshire fog), Agrostis gens, exposure to pollen grains depending of the capillaris syn. Agrostis vulgaris (bent grass), and Ar- type of plant, wild spread or cultivation, geographic rhenatherum elatius syn. Helictotrichon elatius (oat grass). area, altitude, air currents, temperature, precipita- Allergists should also consider that the grass pollen tion and other weather events, and pollen extracts individual extracts or mixes selected for warm tem- for European and North American skin testing pan- perate and subtropical areas in Europe should cover els are discussed below1-3,6-8,17,35-39. the regionally most dominant grasses, including In the European standard panel, pollen extracts those which are not cross-reactive with Pooideae, such from trees (mostly) or shrubs (some) belong to the as Paspalum notatum (Bahia grass) or Cynodon dactylon class Magnoliopsida (dicotyledons), Betulaceae family: (Bermuda grass). In the panel of clinically relevant Betula pendula syn. Betula verrucosa (European silver aeroallergens of North America, grass pollen extracts birch) or Betula pubescens syn. Betula alba (European belong to the Pooideae subfamily: Phleum pratense (tim- white birch), Alnus glutinosa (European black alder) othy grass), Lolium perenne (ryegrass), Festuca elatior or Alnus incana (grey alder), and Corylus avellana (Eu- (meadow fescue), Chloridoideae subfamily: Cynodon ropean hazel); the Oleaceae family: Olea europaea dactylon (Bermuda grass), and Panicoideae subfamily: (common olive) or Fraxinus excelsior (European ash); Sorghum halepense (Johnson grass), Paspalum notatum Platanaceae family: Platanus acerifolia syn. Platanus vul- (Bahia grass). garis (London plane tree or maple leaf sycamore); In Europe, the skin prick panel includes the most and to the class Coniferopsida (gymnospermae) from important weed pollen extracts involved in allergic the Cupressaceae family: Cupressus sempervirens (Medi- rhinitis belonging to herbaceous plants from the terranean cypress). In the North American list of class Magnoliopsida (dicotyledons), Asterales order, major clinically relevant aeroallergens, Magnoliopsida Asteraceae / Compositae family: Ambrosia artemisiifolia trees/shrubs pollen extracts belong to the Betulaceae var. elatior (short ragweed or common ragweed), Ar- family: Betula papyrifera (paper birch), Alnus rubra temisia vulgaris (mugwort or common wormwood), (red alder); Fagaceae family: Quercus alba (white oak), and Rosales order, Urticaceae family: Parietaria offici- Quercus rubra (Northern red oak); Juglandaceae fam- nalis (wall pellitory or lichwort) or Parietaria judaica ily: Juglans nigra (black walnut), Carya illinoinensis (wall pellitory or sticky weed). Weed pollen from (pecan tree); Salicaceae family: Populus deltoides (East- Amaranthaceae/Chenopodiaceae family, Chenopodium ern cottonwood); Oleaceae family: Fraxinus americana album (lamb’s quarter or fat hen white goosefoot) (white ash), Olea europaea (common olive); Platan- and Salsola kali (Russian thistle or common saltwort) aceae family: Platanus occidentalis (American syca- are important pollen aeroallergens in Spain and more); Aceraceae family: Acer rubrum (red maple) or semi-arid areas. Some experts mention adding Plan- Acer negundo (boxelder maple); Moraceae family: tago lanceolata (narrow-leaved plantain) from Plan- Morus rubra (red mulberry); and Ulmaceae family: taginaceae family, to Chenopodium sp and Salsola kali, Ulmus americana (American elm), Ulmus pumila (Sibe- for routine aeroallergen regional panels in countries rian elm) or Ulmus parvifolia (Chinese elm). Juniperus like Turkey, Spain, Italy and Greece. It is important ashei (mountain cedar) pollen extract included in the to test these allergens depending on local climate, North American list is a standard of the Cuppressaceae but possibly not to use them in a pan-European skin family. test battery. Moreover, the GA2LEN skin tests may be Grass pollen is produced in Europe by wild or cul- extended to other parts of the world to assess the tivated herbaceous plants belonging to class Liliopsida common panel for skin testing. The North American (monocotyledons), Poales order, Poaceae family Practice Parameters skin prick panel includes weed (gramineae). The European standards for the skin pollen extracts belonging to Asterales order, Asteraceae prick testing recommend a pollen mix of five grasses family: Ambrosia artemisiifolia (short ragweed), Artemi- belonging to Pooideae subfamily. Phleum pratense (tim- sia vulgaris (mugwort); Lamiales order, Plantaginaceae othy grass), Dactylis glomerata (orchard grass or cock’s family: Plantago lanceolata (narrow-leaved plantain); foot grass), Poa pratensis (smooth meadow grass or Caryophyllales order, Polygonaceae family: Rumex aceto- bluegrass), Lolium perenne (perennial ryegrass) and sella (sheep sorrel) and Amaranthaceae family: Ama- Anthoxanthum odoratum (sweet vernal grass) are wide- ranthus retroflexus (redroot pigweed), Salsola kali (Rus- 22 Romanian Journal of Rhinology, Vol. 5, No. 17, January-March 2015

Asthma and Immunology - Allergy diagnostic testing: an updated prac- sian thistle or common saltwort) and Bassia scoparia tice parameter. Ann Allergy Asthma Immunol., 2008;100(3 Suppl 3):S1- syn. Kochia scoparia (burning bush). 148. It is important to underline that the American 4. Heinzerling L., Frew A.J., Bindslev-Jensen C., Bonini S., Bousquet J., Academy of Allergy, Asthma and Immunology Bresciani M., Carlsen K.H., van Cauwenberge P., Darsow U., Fokkens W., (AAAAI) selected the above mentioned 36 major Haahtela T., van Hoecke H., Jessberger B., Kowalski M.L., Kopp T., clinically relevant aeroallergens for North America3, Lahoz C.N., Lodrup Carlsen K.C., Papadopoulos N.G., Ring J., Schmid- while in the United States, according to the third Na- Grendelmeier P., Vignola A.M., Wöhrl S., Zuberbier T. - Standard skin tional Health and Nutrition Examination Surveys prick testing and sensitization to inhalant allergens across Europe - a (NHANES), few aeroallergen extracts were previ- survey from the GA2LEN network. Allergy, 2005;60(10):1287-1300. ously used for skin testing screening: Dermatophagoides 5. Heinzerling L.M., Burbach G.J., Edenharter G., Bachert C., Bindslev- spp (dust mites), Blattella germanica (German cock- Jensen C., Bonini S., Bousquet J., Bousquet-Rouanet L., Bousquet P.J., roach), Felis domesticus (cat), Alternaria alternata, and Bresciani M., Bruno A., Burney P., Canonica G.W., Darsow U., Demoly pollen from Quercus alba (white oak), Lolium perenne P., Durham S., Fokkens W.J., Giavi S., Gjomarkaj M., Gramiccioni C., (perennial rye), Cynodon dactylon (Bermuda grass), Haahtela T., Kowalski M.L., Magyar P., Muraközi G., Orosz M., Ambrosia eliator (short ragweed), Salsola kali (Russian Papadopoulos N.G., Rohnelt C., Stingl G., Todo-Bom A., von Mutius E., thistle)40. Wiesner A., Wöhrl S., Zuberbier T. - GA2LEN skin test study I: GA2LEN harmonization of skin prick testing: novel sensitization patterns for inhal- CONCLUSIONS ant allergens in Europe. Allergy, 2009;64(10):1498-1506. 6. Passali D., Bellusi L.M., Kern E.B., Sarafoleanu C., Popescu F.D. - Rhinosinusal inflammation and infections: modern thinking and current In conclusion, allergists and ENT specialists from treatment. Editura Academiei Romane, Bucharest, 2013;p.101-167. the Northern Hemisphere must be informed regard- 7. Haahtela T., Burbach G.J., Bachert C., Bindslev-Jensen C., Bonini S., ing the European standards and North American Bousquet J., Bousquet-Rouanet L., Bousquet P.J., Bresciani M., Bruno A., practice parameters for skin prick panels of aeroal- Canonica G.W., Darsow U., Demoly P., Durham S.R., Fokkens W.J., Giavi lergens of plant, fungal and animal origins, used in S., Gjomarkaj M., Gramiccioni C., Kowalski M.L., Losonczy G., Orosz M., the diagnosis of allergic rhinitis with asthma. The Papadopoulos N.G., Stingl G., Todo-Bom A., von Mutius E., Köhli A., GA2LEN position statement and AAAAI practice pa- Wohrl S., Jarvenpaa S., Kautiainen H., Petman L., Selroos O., Zuberbier rameters regarding skin prick testing to aeroaller- T., Heinzerling L.M. - Clinical relevance is associated with allergen-specific gens were received with great interest by specialists wheal size in skin prick testing. Clin Exp Allergy, 2014 Mar;44(3):407-16. interested in the updated diagnosis of respiratory 8. Popescu F.D., Tamiian M., Albert K. - Multilingual approach to the panel allergies. of aeroallergens suggested for skin prick testing in European Union patients. Romanian Journal of Rhinology, 2014;14(4):93-98. REFERENCES 9. Popescu F.D., Secureanu F.A., Tudose A.M., Tanasescu R.A. - Modificările climei şi alergia la polen. Journal of the Romanian Society of Allergy and Clinical Immunology., 2007;3:112-115. 1. Bousquet J., Heinzerling L., Bachert C., Papadopoulos N.G., Bousquet 10. D’Amato G., Cecchi L. - Effects of climate change on environmental fac- P.J., Burney P.G., Canonica G.W., Carlsen K.H., Cox L., Haahtela T., tors in respiratory allergic diseases. Clin Exp Allergy, 2008;38(8):1264- Lodrup Carlsen K.C., Price D., Samolinski B., Simons F.E., Wickman M., 1274. Annesi-Maesano I., Baena-Cagnani C.E., Bergmann K.C., Bindslev-Jensen 11. Beggs P.J. - Impacts of climate change on aeroallergens: past and future. C., Casale T.B., Chiriac A., Cruz A.A., Dubakiene R., Durham S.R., Clin Exp Allergy, 2004;34(10):1507-1513. Fokkens W.J., Gerth-van-Wijk R., Kalayci O., Kowalski M.L., Mari A., 12. Cecchi L., D’Amato G., Ayres J.G., Galan C., Forastiere F., Forsberg B., Mullol J., Nazamova-Baranova L., O’Hehir R.E., Ohta K., Panzner P., Gerritsen J., Nunes C., Behrendt H., Akdis C., Dahl R., Annesi-Maesano Passalacqua G., Ring J., Rogala B., Romano A., Ryan D., Schmid- I. - Projections of the effects of climate change on allergic asthma: the Grendelmeier P., Todo-Bom A., Valenta R., Woehrl S., Yusuf O.M., contribution of aerobiology. Allergy, 2010;65(9):1073-1081. Zuberbier T., Demoly P.; Global Allergy and Asthma European Network; 13. Wayne P., Foster S., Connolly J., Bazzaz F., Epstein P. - Production of al- Allergic Rhinitis and its Impact on Asthma - Practical guide to skin prick lergenic pollen by ragweed (Ambrosia artemisiifolia L.) is increased in tests in allergy to aeroallergens. Allergy, 2012;67(1):18-24. CO2-enriched atmospheres. Ann Allergy Asthma Immunol., 2. Heinzerling L., Mari A., Bergmann K.C., Bresciani M., Burbach G., 2002;88(3):279-282. Darsow U., Durham S., Fokkens W., Gjomarkaj M., Haahtela T., Bom 14. Ziska L.H., Gebhard D.E., Frenz D.A., Faulkner S., Singer B.D., Straka A.T., Wohrl S., Maibach H., Lockey R. – The skin prick test – European J.G. - Cities as harbingers of climate change: common ragweed, urbaniza- standards. Clin Transl Allergy, 2013;3:3. tion, and public health. J Allergy Clin Immunol., 2003;111(2):290-295. 3. Bernstein I.L., Li J.T., Bernstein D.I., Hamilton R., Spector S.L., Tan R., 15. Galán C., García-Mozo H., Vázquez L., Ruiz L., de la Guardia C.D., Trigo Sicherer S., Golden D.B., Khan D.A., Nicklas R.A., Portnoy J.M., Blessing- M.M. - Heat requirement for the onset of the Olea europaea L. pollen Moore J., Cox L., Lang D.M., Oppenheimer J., Randolph C.C., Schuller season in several sites in Andalusia and the effect of the expected future D.E., Tilles S.A., Wallace D.V., Levetin E., Weber R.; American Academy climate change. Int J Biometeorol., 2005;49(3):184-188. of Allergy, Asthma and Immunology; American College of Allergy, Popescu European standards and North American practice parameters for skin prick testing panels in allergic rhinitis and asthma 23

16. Bartra J., Mullol J., del Cuvillo A., Davila I., Ferrer M., Jauregui I., 25. Fu R.L., Liu Z.G., Xing M., Li L., Zou Z.H. - Antigenic localization of Montoro J., Sastre J., Valero A. - Air pollution and allergens. J Investig specific allergen in the body of Dermatophagoides pteronyssinus by immuno- Allergol Clin Immunol., 2007;17 Suppl 2:3-8. histochemistry. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing 17. Bousquet J., Khaltaev N., Cruz A.A., Denburg J., Fokkens W.J., Togias A., Za Zhi., 2004;22(4):243-244. Zuberbier T., Baena-Cagnani C.E., Canonica G.W., van Weel C., Agache 26. Popescu F.D., Stanescu A.B., Secureanu F.A. - Alergia la Blattella german- I., Aït-Khaled N., Bachert C., Blaiss M.S., Bonini S., Boulet L.P., Bousquet ica. Journal of the Romanian Society of Allergy and Clinical Immunology., P.J., Camargos P., Carlsen K.H., Chen Y., Custovic A., Dahl R., Demoly P., 2009;6(1):3-6. Douagui H., Durham S.R., van Wijk R.G., Kalayci O., Kaliner M.A., Kim 27. Dutau G., Rancé F. - “NPAs”: a new allergic risk? Arch Pediatr., Y.Y., Kowalski M.L., Kuna P., Le L.T., Lemiere C., Li J., Lockey R.F., 2009;16(4):396-401. Mavale-Manuel S., Meltzer E.O., Mohammad Y., Mullol J., Naclerio R., 28. Vieru M., Popescu F.D., Bordeianu I. - Acarienii din genul Blomia ca surse O’Hehir R.E., Ohta K., Ouedraogo S., Palkonen S., Papadopoulos N., de alergene. Journal of the Romanian Society of Allergy and Clinical Passalacqua G., Pawankar R., Popov T.A., Rabe K.F., Rosado-Pinto J., Immunology, 2009;6(2):31-33. Scadding G.K., Simons F.E., Toskala E., Valovirta E., van Cauwenberge 29. Bessot J.C., Pauli G. - Mite allergens: an overview. Eur Ann Allergy Clin P., Wang D.Y., Wickman M., Yawn B.P., Yorgancioglu A., Yusuf O.M., Zar Immunol., 2011;43(5):141-156. H., Annesi-Maesano I., Bateman E.D., Ben Kheder A., Boakye D.A., 30. Renström A., Olsson M., Hedrén M., Johansson S.G., van Hage M. - Pet Bouchard J., Burney P., Busse W.W., Chan-Yeung M., Chavannes N.H., shop workers: exposure, sensitization, and work-related symptoms. Chuchalin A., Dolen W.K., Emuzyte R., Grouse L., Humbert M., Jackson Allergy, 2011;66(8):1081-1087. C., Johnston S.L., Keith P.K., Kemp J.P., Klossek J.M., Larenas-Linnemann 31. Green B.J., Tovey E.R., Sercombe J.K., Blachere F.M., Beezhold D.H., D., Lipworth B., Malo J.L., Marshall G.D., Naspitz C., Nekam K., Schmechel D. - Airborne fungal fragments and allergenicity. Med Mycol., Niggemann B., Nizankowska-Mogilnicka E., Okamoto Y., Orru M.P., 2006;44:S245-255. Potter P., Price D., Stoloff S.W., Vandenplas O., Viegi G., Williams D.; 32. Simon-Nobbe B., Denk U., Pöll V., Rid R., Breitenbach M. - The spec- World Health Organization; GA2LEN; AllerGen. - AR and its Impact on trum of fungal allergy. Int Arch Allergy Immunol., 2008;145(1):58-86. Asthma (ARIA) 2008 update (in collaboration with the World Health 33. Crameri R., Zeller S., Glaser A.G., Vilhelmsson M., Rhyner C. - Cross- Organization, GA2LEN and AllerGen). Allergy, 2008;63 Suppl 86:8-160. reactivity among fungal allergens: a clinically relevant phenomenon? 18. Frei T., Gassner E. - Climate change and its impact on birch pollen quan- Mycoses, 2009;52(2):99-106. tities and the start of the pollen season an example from Switzerland for 34. Torres-Rodríguez J.M., Pulido-Marrero Z., Vera-García Y. - Respiratory the period 1969-2006. Int J Biometeorol., 2008;52(7):667-674. allergy to fungi in Barcelona, Spain: Clinical aspects, diagnosis and spe- 19. García-Mozo H., Chuine I., Aira M.J., Belmonte J., Bermejo D., Díaz de cific treatment in a general allergy unit. Allergol Immunopathol (Madr)., la Guardia C., Elvira B., Gutiérrez M., Rodríguez-Rajo J., Ruiz L., Trigo 2012;40(5):295-300. M.M., Tormo R., Valencia R., Galán C. - Regional phenological models 35. D’Amato G., Cecchi L., Bonini S., Nunes C., Annesi-Maesano I., Behrendt for forecasting the start and peak of the Quercus pollen season in Spain. H., Liccardi G., Popov T., van Cauwenberge P. - Allergenic pollen and Agricultural and Forest Meteorology., 2008;148:372-380. pollen allergy in Europe. Allergy, 2007;62(9):976-990. 20. de Weger L.A., Hiemstra P.S. - The effect of climate change on pollen 36. Grote M., Westritschnig K., Valenta R. - Immunogold electron micro- allergy in the Netherlands. Ned Tijdschr Geneeskd., 2009;153:A1410. scopic localization of the 2 EF-hand calcium-binding pollen allergen Phl 21. García-Mozo H., Galán C., Belmonte J., Bermejo D., Candau P., Díaz de p 7 and its homologues in pollens of grasses, weeds and trees. Int Arch la Guardia C., Elvira B., Gutiérrez M., Jato V., Silva I., Trigo M.M., Allergy Immunol., 2008;146(2):113-121. Valencia R., Chuine I. - Predicting the start and peak dates of the Poaceae 37. Takhtajan A. - Flowering Plants. Second Edition. Springer, 2009;pp.1- pollen season in Spain using process-based models. Agriculture and 750. Forest Meteorology., 2009;149:256-262. 38. Popescu F.D., Tudose A.M. - Ambrosia pollen sensitization in allergic pa- 22. Sommer J., Plaschke P., Poulsen L.K. - Allergic disease-pollen allergy and tients from the central part of the Romanian Plain. Romanian Journal of climate change. Ugeskr Laeger., 2009 Oct 26;171(44):3184-3187. Rhinology, 2011;1(1):26-30. 23. Fotiou C., Damialis A., Krigas N., Halley J.M., Vokou D. - Parietaria judaica 39. Sekerel B.E., Sahiner U.M., Bousquet J., Demoly P., Zuberbier T., Carlsen flowering phenology, pollen production, viability and atmospheric circu- K.H., Wickman M. - Practical guide to skin prick tests in allergy to aeroal- lation, and expansive ability in the urban environment: impacts of envi- lergens: some concerns. Allergy, 2012;67(3):442; author reply 443. ronmental factors. Int J Biometeorol., 2011;55(1):35-50. 40. Arbes S.J. Jr, Gergen P.J., Elliott L., Zeldin D.C. - Prevalences of positive 24. Ziska L., Knowlton K., Rogers C., Dalan D., Tierney N., Elder M.A., Filley skin test responses to 10 common allergens in the US population: results W., Shropshire J., Ford L.B., Hedberg C., Fleetwood P., Hovanky K.T., from the third National Health and Nutrition Examination Survey. J Kavanaugh T., Fulford G., Vrtis R.F., Patz J.A., Portnoy J., Coates F., Allergy Clin Immunol., 2005;116:377-383. Bielory L., Frenz D. - Recent warming by latitude associated with increased length of ragweed pollen season in central North America. Proc Natl Acad Sci U S A., 2011;108(10):4248-4251.